{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,9]],"date-time":"2026-09-09T01:06:56Z","timestamp":1788916016999,"version":"build-2803163510"},"reference-count":67,"publisher":"Wiley","issue":"5","license":[{"start":{"date-parts":[[2026,9,8]],"date-time":"2026-09-08T00:00:00Z","timestamp":1788825600000},"content-version":"vor","delay-in-days":7,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T00:00:00Z","timestamp":1788220800000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"funder":[{"DOI":"10.13039\/100019180","name":"HORIZON EUROPE European Research Council","doi-asserted-by":"publisher","award":["101003304"],"award-info":[{"award-number":["101003304"]}],"id":[{"id":"10.13039\/100019180","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Physiologia Plantarum"],"published-print":{"date-parts":[[2026,9]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>\n                    Arbuscular mycorrhizal fungi (AMF) form symbiotic associations with plant roots, profoundly shaping root system architecture (RSA) and influencing nutrient acquisition in crops. This modulation begins during the early pre\u2010symbiotic stage, when plants and fungi interact without physical contact. Root formation is orchestrated by signaling molecules, including hormones such as auxin (IAA) and strigolactones (SLs), as well as reactive nitrogen species such as nitric oxide (NO). However, the mechanisms by which AMF spores modulate these pathways to influence root development in rice remain largely unexplored. Here, we investigated the effects of\n                    <jats:italic>Rhizophagus irregularis<\/jats:italic>\n                    spores on root formation in\n                    <jats:styled-content style=\"fixed-case\">\n                      <jats:italic>Oryza sativa<\/jats:italic>\n                    <\/jats:styled-content>\n                    L., focusing on IAA, SLs, and NO modulation. Exposure to both live and autoclaved spores enhanced lateral root formation in adventitious roots, whereas only live spores promoted elongation and secondary branching of large lateral roots (LLRs), a rice\u2010specific feature. These effects were correlated with increased IAA levels, transcriptomic changes, and decreased SL accumulation, revealing an integrated signaling network controlling LLR development. Histochemical analyses revealed NO accumulation in the root elongation zone and apex, accompanied by the upregulation of the high\u2010affinity nitrate transporter\n                    <jats:italic>OsNRT2.1<\/jats:italic>\n                    in LLRs. Together, our findings reveal a root\u2010type\u2010specific involvement of IAA, SLs, and NO in shaping RSA during the pre\u2010symbiotic stage of AMF interactions. This study provides new insights into early signaling events that mediate host discrimination and regulate root architecture during the pre\u2010symbiotic phase of AMF establishment.\n                  <\/jats:p>","DOI":"10.1111\/ppl.71099","type":"journal-article","created":{"date-parts":[[2026,9,9]],"date-time":"2026-09-09T00:16:17Z","timestamp":1788912977000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Auxin, Strigolactones, and Nitric Oxide Coordinate Lateral Root Development in Rice During Early Interaction With\n                    <i>Rhizophagus irregularis<\/i>"],"prefix":"10.1111","volume":"178","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5016-1983","authenticated-orcid":false,"given":"Giulia","family":"Raffaele","sequence":"first","affiliation":[{"name":"Bioinspired Soft Robotics Laboratory Istituto Italiano di Tecnologia  Genova Italy"},{"name":"Department of Science and Bio\u2010Technology Universit\u00e0 Campus Bio\u2010Medico di Roma  Rome Italy"},{"name":"Department of Biology Universit\u00e0 degli Studi di Napoli Federico II  Napoli Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5349-8146","authenticated-orcid":false,"given":"Marilena","family":"Ronzan","sequence":"additional","affiliation":[{"name":"Bioinspired Soft Robotics Laboratory Istituto Italiano di Tecnologia  Genova Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6874-1970","authenticated-orcid":false,"given":"Emanuela","family":"Del Dottore","sequence":"additional","affiliation":[{"name":"Bioinspired Soft Robotics Laboratory Istituto Italiano di Tecnologia  Genova Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0779-474X","authenticated-orcid":false,"given":"Jian You","family":"Wang","sequence":"additional","affiliation":[{"name":"The BioActives Lab King Abdullah University of Science and Technology  Thuwal Saudi Arabia"},{"name":"Agricultural Biotechnology Research Center Academia Sinica  Taipei Taiwan"},{"name":"Biotechnology Center in Southern Taiwan Academia Sinica  Tainan Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6457-751X","authenticated-orcid":false,"given":"Paolo","family":"Bianchini","sequence":"additional","affiliation":[{"name":"Nanoscopy and NIC@IIT Istituto Italiano di Tecnologia  Genova Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4916-5928","authenticated-orcid":false,"given":"Alberto","family":"Diaspro","sequence":"additional","affiliation":[{"name":"Nanoscopy and NIC@IIT Istituto Italiano di Tecnologia  Genova Italy"},{"name":"DIFILAB, Department of Physics Universit\u00e0 di Genova  Genova Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carlo","family":"Filippeschi","sequence":"additional","affiliation":[{"name":"Bioinspired Soft Robotics Laboratory Istituto Italiano di Tecnologia  Genova Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4823-2882","authenticated-orcid":false,"given":"Salim","family":"Al\u2010Babili","sequence":"additional","affiliation":[{"name":"The BioActives Lab King Abdullah University of Science and Technology  Thuwal Saudi Arabia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5938-7113","authenticated-orcid":false,"given":"Laura","family":"De Gara","sequence":"additional","affiliation":[{"name":"Department of Science and Bio\u2010Technology Universit\u00e0 Campus Bio\u2010Medico di Roma  Rome Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0722-8350","authenticated-orcid":false,"given":"Barbara","family":"Mazzolai","sequence":"additional","affiliation":[{"name":"Bioinspired Soft Robotics Laboratory Istituto Italiano di Tecnologia  Genova Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,9,8]]},"reference":[{"key":"e_1_2_11_2_1","doi-asserted-by":"crossref","first-page":"824","DOI":"10.1038\/nature03608","article-title":"Plant Sesquiterpenes Induce Hyphal Branching in Arbuscular Mycorrhizal Fungi","volume":"435","author":"Akiyama K.","year":"2005","journal-title":"Nature"},{"key":"e_1_2_11_3_1","doi-asserted-by":"crossref","DOI":"10.3390\/plants12020413","article-title":"New Paradigms in Brassinosteroids, Strigolactones, Sphingolipids, and Nitric Oxide Interaction in the Control of Lateral and Adventitious Root Formation","volume":"12","author":"Altamura M. 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D. W EIGEL & J. G LAZEBROOK","volume":"80","author":"Goodrich J.","year":"2002","journal-title":"Genetical Research"},{"key":"e_1_2_11_25_1","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1111\/j.1469-8137.2009.02839.x","article-title":"Glomus Intraradices Induces Changes in Root System Architecture of Rice Independently of Common Symbiosis Signaling","volume":"182","author":"Gutjahr C.","year":"2009","journal-title":"New Phytologist"},{"key":"e_1_2_11_26_1","doi-asserted-by":"crossref","first-page":"701","DOI":"10.1111\/j.1469-8137.2010.03567.x","article-title":"Genetic Evidence for Auxin Involvement in Arbuscular Mycorrhiza Initiation","volume":"189","author":"Hanlon M. 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G.","year":"2010","journal-title":"Plant Journal"},{"key":"e_1_2_11_30_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2024.1343928","article-title":"Modulating Root System Architecture: Cross\u2010Talk Between Auxin and Phytohormones","volume":"15","author":"Jan M.","year":"2024","journal-title":"Frontiers in Plant Science"},{"key":"e_1_2_11_31_1","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.2101846119","article-title":"WUSCHEL\u2010Related Homeobox Family Genes in Rice Control Lateral Root Primordium Size","volume":"119","author":"Kawai T.","year":"2022","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"key":"e_1_2_11_32_1","doi-asserted-by":"crossref","first-page":"544","DOI":"10.1093\/pcp\/pcy001","article-title":"Strigolactone Biosynthesis Genes of Rice Are Required for the Punctual Entry of Arbuscular Mycorrhizal Fungi Into the Roots","volume":"59","author":"Kobae Y.","year":"2018","journal-title":"Plant & Cell Physiology"},{"key":"e_1_2_11_33_1","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1111\/ppl.12823","article-title":"Control of Adventitious Root Formation: Insights Into Synergistic and Antagonistic Hormonal Interactions","volume":"165","author":"Lakehal A.","year":"2019","journal-title":"Physiologia Plantarum"},{"key":"e_1_2_11_34_1","doi-asserted-by":"crossref","first-page":"2175","DOI":"10.1093\/jxb\/erx432","article-title":"Strigolactones Cross the Kingdoms: Plants, Fungi, and Bacteria in the Arbuscular Mycorrhizal Symbiosis","volume":"69","author":"Lanfranco L.","year":"2018","journal-title":"Journal of Experimental Botany"},{"key":"e_1_2_11_35_1","doi-asserted-by":"crossref","DOI":"10.1126\/sciadv.adq3942","article-title":"OsCYP706C2 Diverts Rice Strigolactone Biosynthesis to a Noncanonical Pathway Branch","volume":"10","author":"Li C.","year":"2024","journal-title":"Science Advances"},{"key":"e_1_2_11_36_1","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1093\/jxb\/erad263","article-title":"Signal Communication During Microbial Modulation of Root System Architecture","volume":"75","author":"Li Y.","year":"2024","journal-title":"Journal of Experimental Botany"},{"key":"e_1_2_11_37_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.rhisph.2022.100632","article-title":"Role of Auxin in the Symbiotic Relationship Between Piriformospora Indica and Rice Plants","volume":"25","author":"Lin P.\u2010C.","year":"2023","journal-title":"Rhizosphere"},{"key":"e_1_2_11_38_1","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1016\/j.scienta.2018.02.052","article-title":"Mycorrhiza\u2010Induced Change in Root Hair Growth is Associated With IAA Accumulation and Expression of EXPs in Trifoliate Orange Under Two P Levels","volume":"234","author":"Liu C. Y.","year":"2018","journal-title":"Scientia Horticulturae"},{"key":"e_1_2_11_39_1","doi-asserted-by":"crossref","first-page":"4875","DOI":"10.1093\/jxb\/ers166","article-title":"Nitric Oxide Is Essential for Vesicle Formation and Trafficking in Arabidopsis Root Hair Growth","volume":"63","author":"Lombardo M. C.","year":"2012","journal-title":"Journal of Experimental Botany"},{"key":"e_1_2_11_40_1","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1007\/978-90-481-9489-6_8","volume-title":"Arbuscular Mycorrhizas: Physiology and Function","author":"Ludwig\u2010M\u00fcller J.","year":"2010"},{"key":"e_1_2_11_41_1","doi-asserted-by":"crossref","first-page":"1560","DOI":"10.1111\/nph.15898","article-title":"Nitric Oxide and Phytoglobin PHYTOGB1 Are Regulatory Elements in the \n                     Solanum lycopersicum\n                  \u2014Rhizophagus Irregularis Mycorrhizal Symbiosis","volume":"223","author":"Mart\u00ednez\u2010Medina A.","year":"2019","journal-title":"New Phytologist"},{"key":"e_1_2_11_42_1","doi-asserted-by":"crossref","first-page":"4489","DOI":"10.1093\/jxb\/erz289","article-title":"Nitric Oxide in Plant\u2013Fungal Interactions","volume":"70","author":"Mart\u00ednez\u2010Medina A.","year":"2019","journal-title":"Journal of Experimental Botany"},{"key":"e_1_2_11_43_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.crmicr.2021.100026","article-title":"Involvement of Strigolactone Hormone in Root Development, Influence and Interaction With Mycorrhizal Fungi in Plant: Mini\u2010Review","volume":"2","author":"Mitra D.","year":"2021","journal-title":"Current Research in Microbial Sciences"},{"key":"e_1_2_11_44_1","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1111\/j.1399-3054.1962.tb08052.x","article-title":"A Revised Medium for Rapid Growth and Bio Assays With Tobacco Tissue Cultures","volume":"15","author":"Murashige T.","year":"1962","journal-title":"Physiologia Plantarum"},{"key":"e_1_2_11_45_1","doi-asserted-by":"crossref","first-page":"1145","DOI":"10.1093\/bbb\/zbad089","article-title":"Molecular and Cellular Insights Into Auxin\u2010Regulated Primary Root Growth: A Comparative Study of Arabidopsis and Rice","volume":"87","author":"Nakamura A.","year":"2023","journal-title":"Bioscience, Biotechnology, and Biochemistry"},{"key":"e_1_2_11_46_1","doi-asserted-by":"crossref","DOI":"10.3390\/genes10040290","article-title":"Overexpression of Nitrate Transporter OsNRT2.1 Enhances Nitrate\u2010Dependent Root Elongation","volume":"10","author":"Naz M.","year":"2019","journal-title":"Genes"},{"key":"e_1_2_11_47_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2020.01019","article-title":"Strigolactones Interact With Nitric Oxide in Regulating Root System Architecture of \n                     Arabidopsis thaliana","volume":"11","author":"Ol\u00e1h D.","year":"2020","journal-title":"Frontiers in Plant Science"},{"key":"e_1_2_11_48_1","article-title":"Emerging Roles of Strigolactones in Plant Responses to Stress and Development","volume":"7","author":"Pandey A.","year":"2016","journal-title":"Frontiers in Plant Science"},{"key":"e_1_2_11_49_1","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1093\/jxb\/erad399","article-title":"The Emerging Roles of Nitric Oxide and Its Associated Scavengers\u2014Phytoglobins\u2014In Plant Symbiotic Interactions","volume":"75","author":"Pathak P. 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